The staphylococcal surface-glycopolymer wall teichoic acid (WTA) is crucial for complement activation and immunological defense against Staphylococcus aureus infection

Immunobiology

Volumn 221, Issue 10, 2016, Pages 1091-1101

  Kurokawa, Kenji ^a   Takahashi, Kazue ^b   Lee, Bok Luel ^c  

^a NAGASAKI INTERNATIONAL UNIVERSITY   (Japan)

^b MASSACHUSETTS GENERAL HOSPITAL   (United States)

^c Pusan National University   (South Korea)

Author keywords

Classical pathway; Complement; MBL; Opsonophagocytosis; Staphylococcus aureus; Wall teichoic acid

Indexed keywords

AMYLOID; EPITOPE; IMMUNOGLOBULIN G; PEPTIDOGLYCAN; SERUM AMYLOID COMPONENT P; TEICHOIC ACID; UNCLASSIFIED DRUG; WALL TEICHOIC ACID; BACTERIAL POLYSACCHARIDE; BACTERIUM ANTIBODY; COMPLEMENT; MANNOSE BINDING LECTIN; OPSONIN; PROTEIN BINDING; SERUM AMYLOID P;

ADAPTIVE IMMUNITY; BACTERIAL CELL; BINDING AFFINITY; CELL SURFACE; COMPLEMENT ACTIVATION; HOST RESISTANCE; HUMAN; IMMUNIZATION; IMMUNOGLOBULIN BLOOD LEVEL; METHICILLIN RESISTANT STAPHYLOCOCCUS AUREUS INFECTION; MOLECULAR RECOGNITION; NONHUMAN; PHAGOCYTOSIS; PRIORITY JOURNAL; PROTEIN BLOOD LEVEL; REINFECTION; REVIEW; STAPHYLOCOCCUS INFECTION; AGE; ANIMAL; BLOOD; CELL WALL; CHEMISTRY; HOST PATHOGEN INTERACTION; IMMUNOLOGY; METABOLISM; MICROBIOLOGY; STAPHYLOCOCCUS AUREUS;

ADAPTIVE IMMUNITY; AGE FACTORS; ANIMALS; ANTIBODIES, BACTERIAL; CELL WALL; COMPLEMENT ACTIVATION; COMPLEMENT SYSTEM PROTEINS; EPITOPES; HOST-PATHOGEN INTERACTIONS; HUMANS; IMMUNIZATION; IMMUNOGLOBULIN G; MANNOSE-BINDING LECTIN; OPSONIN PROTEINS; PHAGOCYTOSIS; POLYSACCHARIDES, BACTERIAL; PROTEIN BINDING; SERUM AMYLOID P-COMPONENT; STAPHYLOCOCCAL INFECTIONS; STAPHYLOCOCCUS AUREUS; TEICHOIC ACIDS;

EID: 84978849134     PISSN: 01712985     EISSN: 18783279     Source Type: Journal    
DOI: 10.1016/j.imbio.2016.06.003     Document Type: Review

References (95)

1. Amano, A., Nakagawa, I., Yoshimori, T., Autophagy in innate immunity against intracellular bacteria. J. Biochem. 140 (2006), 161–166.
2. An, J.H., Kurokawa, K., Jung, D.J., Kim, M.J., Kim, C.H., Fujimoto, Y., Fukase, K., Coggeshall, K.M., Lee, B.L., Human SAP is a novel peptidoglycan recognition protein that induces complement-independent phagocytosis of Staphylococcus aureus. J. Immunol. 191 (2013), 3319–3327.
3. Baldwin, S.L., Bertholet, S., Kahn, M., Zharkikh, I., Ireton, G.C., Vedvick, T.S., Reed, S.G., Coler, R.N., Intradermal immunization improves protective efficacy of a novel TB vaccine candidate. Vaccine 27 (2009), 3063–3071.
4. Barclay, A.N., Hatherley, D., The counterbalance theory for evolution and function of paired receptors. Immunity 29 (2008), 675–678.
5. Baur, S., Rautenberg, M., Faulstich, M., Grau, T., Severin, Y., Unger, C., Hoffmann, W.H., Rudel, T., Autenrieth, I.B., Weidenmaier, C., A nasal epithelial receptor for Staphylococcus aureus WTA governs adhesion to epithelial cells and modulates nasal colonization. PLoS Pathog., 10, 2014, e1004089.
6. Bera, A., Herbert, S., Jakob, A., Vollmer, W., Gotz, F., Why are pathogenic staphylococci so lysozyme resistant? The peptidoglycan O-acetyltransferase OatA is the major determinant for lysozyme resistance of Staphylococcus aureus. Mol. Microbiol. 55 (2005), 778–787.
7. Bottazzi, B., Garlanda, C., Salvatori, G., Jeannin, P., Manfredi, A., Mantovani, A., Pentraxins as a key component of innate immunity. Curr. Opin. Immunol. 18 (2006), 10–15.
8. Brown, S., Xia, G., Luhachack, L.G., Campbell, J., Meredith, T.C., Chen, C., Winstel, V., Gekeler, C., Irazoqui, J.E., Peschel, A., Walker, S., Methicillin resistance in Staphylococcus aureus requires glycosylated wall teichoic acids. Proc. Natl. Acad. Sci. U. S. A. 109 (2012), 18909–18914.
9. Caruso, R., Warner, N., Inohara, N., Nunez, G., NOD1 and NOD2: signaling, host defense, and inflammatory disease. Immunity 41 (2014), 898–908.
10. Cobb, B.A., Wang, Q., Tzianabos, A.O., Kasper, D.L., Polysaccharide processing and presentation by the MHCII pathway. Cell 117 (2004), 677–687.
11. Collard, C.D., Shernan, S.K., Fox, A.A., Bernig, T., Chanock, S.J., Vaughn, W.K., Takahashi, K., Ezekowitz, A.B., Jarolim, P., Body, S.C., The MBL2 ‘LYQA secretor’ haplotype is an independent predictor of postoperative myocardial infarction in whites undergoing coronary artery bypass graft surgery. Circulation 116 (2007), I106–112.
12. Colque-Navarro, P., Jacobsson, G., Andersson, R., Flock, J.I., Mollby, R., Levels of antibody against 11 Staphylococcus aureus antigens in a healthy population. Clin. Vaccine Immunol. 17 (2010), 1117–1123.
13. Daha, N.A., Banda, N.K., Roos, A., Beurskens, F.J., Bakker, J.M., Daha, M.R., Trouw, L.A., Complement activation by (auto-) antibodies. Mol. Immunol. 48 (2011), 1656–1665.
14. DeLeo, F.R., Diep, B.A., Otto, M., Host defense and pathogenesis in Staphylococcus aureus infections. Infect. Dis. Clin. North Am. 23 (2009), 17–34.
15. Dryla, A., Prustomersky, S., Gelbmann, D., Hanner, M., Bettinger, E., Kocsis, B., Kustos, T., Henics, T., Meinke, A., Nagy, E., Comparison of antibody repertoires against Staphylococcus aureus in healthy individuals and in acutely infected patients. Clin. Diagn. Lab. Immunol. 12 (2005), 387–398.
16. Dunne, D.W., Resnick, D., Greenberg, J., Krieger, M., Joiner, K.A., The type I macrophage scavenger receptor binds to gram-positive bacteria and recognizes lipoteichoic acid. Proc. Natl. Acad. Sci. U. S. A. 91 (1994), 1863–1867.
17. Ferrandon, D., Imler, J.L., Hetru, C., Hoffmann, J.A., The Drosophila systemic immune response: sensing and signalling during bacterial and fungal infections. Nat. Rev. Immunol. 7 (2007), 862–874.
18. Fischer, W., Lipoteichoic acid and lipids in the membrane of Staphylococcus aureus. Med. Microbiol. Immunol. 183 (1994), 61–76.
19. Foster, T.J., McDevitt, D., Surface-associated proteins of Staphylococcus aureus: their possible roles in virulence. FEMS Microbiol. Lett. 118 (1994), 199–205.
20. Foster, T.J., Immune evasion by staphylococci. Nat. Rev. 3 (2005), 948–958.
21. Fournier, B., Philpott, D.J., Recognition of Staphylococcus aureus by the innate immune system. Clin. Microbiol. Rev. 18 (2005), 521–540.
22. Fowler, V.G. Jr., Proctor, R.A., Where does a Staphylococcus aureus vaccine stand?. Clin. Microbiol. Infect. 20:Suppl. 5 (2014), 66–75.
23. Fraunholz, M., Sinha, B., Intracellular Staphylococcus aureus: live-in and let die. Front. Cell. Infect. Microbiol., 2, 2012, 43.
24. Fu, H., Karlsson, J., Bylund, J., Movitz, C., Karlsson, A., Dahlgren, C., Ligand recognition and activation of formyl peptide receptors in neutrophils. J. Leukoc. Biol. 79 (2006), 247–256.
25. Fujita, T., Evolution of the lectin-complement pathway and its role in innate immunity. Nat. Rev. Immunol. 2 (2002), 346–353.
26. Ghetie, V., Ward, E.S., Multiple roles for the major histocompatibility complex class I-related receptor FcRn. Annu. Rev. Immunol. 18 (2000), 739–766.
27. Grundling, A., Schneewind, O., Genes required for glycolipid synthesis and lipoteichoic acid anchoring in Staphylococcus aureus. J. Bacteriol. 189 (2007), 2521–2530.
28. Guttormsen, H.K., Stuart, L.M., Shi, L., Carroll, M.C., Chen, J., Kasper, D.L., Ezekowitz, R.A., Takahashi, K., Deficiency of mannose-binding lectin greatly increases antibody response in a mouse model of vaccination. Clin. Immunol. (Orlando, Fla) 130 (2009), 264–271.
29. Hajishengallis, G., Lambris, J.D., Microbial manipulation of receptor crosstalk in innate immunity. Nat. Rev. Immunol. 11 (2011), 187–200.
30. Hashimoto, Y., Tabuchi, Y., Sakurai, K., Kutsuna, M., Kurokawa, K., Awasaki, T., Sekimizu, K., Nakanishi, Y., Shiratsuchi, A., Identification of lipoteichoic acid as a ligand for draper in the phagocytosis of Staphylococcus aureus by Drosophila hemocytes. J. Immunol. 183 (2009), 7451–7460.
31. Hauck, C.R., Ohlsen, K., Sticky connections: extracellular matrix protein recognition and integrin-mediated cellular invasion by Staphylococcus aureus. Curr. Opin. Microbiol. 9 (2006), 5–11.
32. Hoffmann, J.A., Kafatos, F.C., Janeway, C.A., Ezekowitz, R.A., Phylogenetic perspectives in innate immunity. Science 284 (1999), 1313–1318.
33. Ip, W.K., Takahashi, K., Moore, K.J., Stuart, L.M., Ezekowitz, R.A., Mannose-binding lectin enhances Toll-like receptors 2 and 6 signaling from the phagosome. J. Exp. Med. 205 (2008), 169–181.
34. Irani, V., Guy, A.J., Andrew, D., Beeson, J.G., Ramsland, P.A., Richards, J.S., Molecular properties of human IgG subclasses and their implications for designing therapeutic monoclonal antibodies against infectious diseases. Mol. Immunol. 67 (2015), 171–182.
35. Iwanaga, S., Lee, B.L., Recent advances in the innate immunity of invertebrate animals. J. Biochem. Mol. Biol. 38 (2005), 128–150.
36. Juergens, W.G., Sanderson, A.R., Strominger, J.L., Chemical basis for an immunological specificity of a strain of Staphylococcus aureus. J. Exp. Med. 117 (1963), 925–935.
37. Jung, D.J., An, J.H., Kurokawa, K., Jung, Y.C., Kim, M.J., Aoyagi, Y., Matsushita, M., Takahashi, S., Lee, H.S., Takahashi, K., Lee, B.L., Specific serum Ig recognizing staphylococcal wall teichoic acid induces complement-mediated opsonophagocytosis against Staphylococcus aureus. J. Immunol. 189 (2012), 4951–4959.
38. Kawai, T., Akira, S., The role of pattern-recognition receptors in innate immunity: update on Toll-like receptors. Nat. Immunol. 11 (2010), 373–384.
39. Kim, J., Yang, J., Park, O.J., Kang, S.S., Kim, W.S., Kurokawa, K., Yun, C.H., Kim, H.H., Lee, B.L., Han, S.H., Lipoproteins are an important bacterial component responsible for bone destruction through the induction of osteoclast differentiation and activation. J. Bone Miner. Res. 28 (2013), 2381–2391.
40. Koch, A., Melbye, M., Sorensen, P., Homoe, P., Madsen, H.O., Molbak, K., Hansen, C.H., Andersen, L.H., Hahn, G.W., Garred, P., Acute respiratory tract infections and mannose-binding lectin insufficiency during early childhood. JAMA 285 (2001), 1316–1321.
41. Kretschmer, D., Gleske, A.K., Rautenberg, M., Wang, R., Koberle, M., Bohn, E., Schoneberg, T., Rabiet, M.J., Boulay, F., Klebanoff, S.J., van Kessel, K.A., van Strijp, J.A., Otto, M., Peschel, A., Human formyl peptide receptor 2 senses highly pathogenic Staphylococcus aureus. Cell Host Microbe 7 (2010), 463–473.
42. Kurokawa, K., Lee, H., Roh, K.B., Asanuma, M., Kim, Y.S., Nakayama, H., Shiratsuchi, A., Choi, Y., Takeuchi, O., Kang, H.J., Dohmae, N., Nakanishi, Y., Akira, S., Sekimizu, K., Lee, B.L., The triacylated ATP binding cluster transporter substrate-binding lipoprotein of staphylococcus aureus functions as a native ligand for toll-like receptor 2. J. Biol. Chem. 284 (2009), 8406–8411.
43. Kurokawa, K., Jung, D.J., An, J.H., Fuchs, K., Jeon, Y.J., Kim, N.H., Li, X., Tateishi, K., Park, J.A., Xia, G., Matsushita, M., Takahashi, K., Park, H.J., Peschel, A., Lee, B.L., Glycoepitopes of staphylococcal wall teichoic acid govern complement-mediated opsonophagocytosis via human serum antibody and mannose-binding lectin. J. Biol. Chem. 288 (2013), 30956–30968.
44. Lacey, K.A., Geoghegan, J.A., McLoughlin, R.M., The role of staphylococcus aureus virulence factors in skin infection and their potential as vaccine antigens. Pathogens, 2016, 5.
45. Le, Y., Murphy, P.M., Wang, J.M., Formyl-peptide receptors revisited. Trends Immunol. 23 (2002), 541–548.
46. Lee, J.H., Kim, N.H., Winstel, V., Kurokawa, K., Larsen, J., An, J.H., Khan, A., Seong, M.Y., Lee, M.J., Andersen, P.S., Peschel, A., Lee, B.L., Surface glycopolymers are crucial for In vitro anti-wall teichoic acid igG-Mediated complement activation and opsonophagocytosis of staphylococcus aureus. Infect. Immun. 83 (2015), 4247–4255.
47. Loffler, B., Tuchscherr, L., Niemann, S., Peters, G., Staphylococcus aureus persistence in non-professional phagocytes. Int. J. Med. Microbiol. 304 (2014), 170–176.
48. Lowy, F.D., Staphylococcus aureus infections. N. Engl. J. Med. 339 (1998), 520–532.
49. Lu, J., Marnell, L.L., Marjon, K.D., Mold, C., Du Clos, T.W., Sun, P.D., Structural recognition and functional activation of FcgammaR by innate pentraxins. Nature 456 (2008), 989–992.
50. Lynch, N.J., Roscher, S., Hartung, T., Morath, S., Matsushita, M., Maennel, D.N., Kuraya, M., Fujita, T., Schwaeble, W.J., L-ficolin specifically binds to lipoteichoic acid, a cell wall constituent of Gram-positive bacteria, and activates the lectin pathway of complement. J. Immunol. 172 (2004), 1198–1202.
51. Ma, Y.G., Cho, M.Y., Zhao, M., Park, J.W., Matsushita, M., Fujita, T., Lee, B.L., Human mannose-binding lectin and L-ficolin function as specific pattern recognition proteins in the lectin activation pathway of complement. J. Biol. Chem. 279 (2004), 25307–25312.
52. Medzhitov, R., Janeway, C.A. Jr., Innate immunity: the virtues of a nonclonal system of recognition. Cell 91 (1997), 295–298.
53. Meister, M., Blood cells of Drosophila: cell lineages and role in host defence. Curr. Opin. Immunol. 16 (2004), 10–15.
54. Merle, N.S., Church, S.E., Fremeaux-Bacchi, V., Roumenina, L.T., Complement system part I—molecular mechanisms of activation and regulation. Front. Immunol., 6, 2015, 262.
55. Michelsen, K.S., Aicher, A., Mohaupt, M., Hartung, T., Dimmeler, S., Kirschning, C.J., Schumann, R.R., The role of toll-like receptors (TLRs) in bacteria-induced maturation of murine dendritic cells (DCS). Peptidoglycan and lipoteichoic acid are inducers of DC maturation and require TLR2. J. Biol. Chem. 276 (2001), 25680–25686.
56. Mohanan, D., Slutter, B., Henriksen-Lacey, M., Jiskoot, W., Bouwstra, J.A., Perrie, Y., Kundig, T.M., Gander, B., Johansen, P., Administration routes affect the quality of immune responses: a cross-sectional evaluation of particulate antigen-delivery systems. J. Control. Release 147 (2010), 342–349.
57. Morse, S.I., Studies on the chemistry and immunochemistry of cell walls of Staphylococcus aureus. J. Exp. Med. 116 (1962), 229–245.
58. Nakayama, H., Kurokawa, K., Lee, B.L., Lipoproteins in bacteria: structures and biosynthetic pathways. FEBS J. 279 (2012), 4247–4268.
59. Nakayama, M., Kurokawa, K., Nakamura, K., Lee, B.L., Sekimizu, K., Kubagawa, H., Hiramatsu, K., Yagita, H., Okumura, K., Takai, T., Underhill, D.M., Aderem, A., Ogasawara, K., Inhibitory receptor paired Ig-like receptor B is exploited by Staphylococcus aureus for virulence. J. Immunol. 189 (2012), 5903–5911.
60. Nathenson, S.G., Strominger, J.L., Enzymatic synthesis and immunochemistry of N-acetylglucosaminylribitol linkages in the teichoic acids of Staphylococcus aureus stains. J. Biol. Chem. 237 (1962), 3839–3841.
61. Navarre, W.W., Schneewind, O., Surface proteins of gram-positive bacteria and mechanisms of their targeting to the cell wall envelope. Microbiol. Mol. Biol. Rev. 63 (1999), 174–229.
62. Neth, O., Jack, D.L., Dodds, A.W., Holzel, H., Klein, N.J., Turner, M.W., Mannose-binding lectin binds to a range of clinically relevant microorganisms and promotes complement deposition. Infect. Immun. 68 (2000), 688–693.
63. Neuhaus, F.C., Baddiley, J., A continuum of anionic charge: structures and functions of D-alanyl-teichoic acids in gram-positive bacteria. Microbiol. Mol. Biol. Rev. 67 (2003), 686–723.
64. Nimmerjahn, F., Ravetch, J.V., Antibody-mediated modulation of immune responses. Immunol. Rev. 236 (2010), 265–275.
65. Oku, Y., Kurokawa, K., Matsuo, M., Yamada, S., Lee, B.L., Sekimizu, K., Pleiotropic roles of poly-glycerolphosphate synthase of lipoteichoic acid in the growth of Staphylococcus aureus cells. J. Bacteriol. 191 (2009), 141–151.
66. Park, K.H., Kurokawa, K., Zheng, L., Jung, D.J., Tateishi, K., Jin, J.O., Ha, N.C., Kang, H.J., Matsushita, M., Kwak, J.Y., Takahashi, K., Lee, B.L., Human serum mannose-binding lectin senses wall teichoic acid Glycopolymer of Staphylococcus aureus, which is restricted in infancy. J. Biol. Chem. 285 (2010), 27167–27175.
67. Peschel, A., Otto, M., Phenol-soluble modulins and staphylococcal infection. Nat. Rev. 11 (2013), 667–673.
68. Peschel, A., Jack, R.W., Otto, M., Collins, L.V., Staubitz, P., Nicholson, G., Kalbacher, H., Nieuwenhuizen, W.F., Jung, G., Tarkowski, A., van Kessel, K.P., van Strijp, J.A., Staphylococcus aureus resistance to human defensins and evasion of neutrophil killing via the novel virulence factor MprF is based on modification of membrane lipids with l-lysine. J. Exp. Med. 193 (2001), 1067–1076.
69. Pluddemann, A., Mukhopadhyay, S., Gordon, S., The interaction of macrophage receptors with bacterial ligands. Expert Rev. Mol. Med. 8 (2006), 1–25.
70. Polotsky, V.Y., Fischer, W., Ezekowitz, R.A., Joiner, K.A., Interactions of human mannose-binding protein with lipoteichoic acids. Infect. Immun. 64 (1996), 380–383.
71. Portoles, M., Kiser, K.B., Bhasin, N., Chan, K.H., Lee, J.C., Staphylococcus aureus Cap5O has UDP-ManNAc dehydrogenase activity and is essential for capsule expression. Infect. Immun. 69 (2001), 917–923.
72. Proctor, R.A., Recent developments for Staphylococcus aureus vaccines: clinical and basic science challenges. Eur. Cell Mater. 30 (2015), 315–326.
73. Ricklin, D., Hajishengallis, G., Yang, K., Lambris, J.D., Complement: a key system for immune surveillance and homeostasis. Nat. Immunol. 11 (2010), 785–797.
74. Rooijakkers, S.H., van Kessel, K.P., van Strijp, J.A., Staphylococcal innate immune evasion. Trends Microbiol. 13 (2005), 596–601.
75. Roumenina, L.T., Ruseva, M.M., Zlatarova, A., Ghai, R., Kolev, M., Olova, N., Gadjeva, M., Agrawal, A., Bottazzi, B., Mantovani, A., Reid, K.B., Kishore, U., Kojouharova, M.S., Interaction of C1q with IgG1, C-reactive protein and pentraxin 3: mutational studies using recombinant globular head modules of human C1q A, B, and C chains. Biochemistry 45 (2006), 4093–4104.
76. Shi, L., Takahashi, K., Dundee, J., Shahroor-Karni, S., Thiel, S., Jensenius, J.C., Gad, F., Hamblin, M.R., Sastry, K.N., Ezekowitz, R.A., Mannose-binding lectin-deficient mice are susceptible to infection with Staphylococcus aureus. J. Exp. Med. 199 (2004), 1379–1390.
77. Shiratsuchi, A., Mori, T., Sakurai, K., Nagaosa, K., Sekimizu, K., Lee, B.L., Nakanishi, Y., Independent recognition of Staphylococcus aureus by two receptors for phagocytosis in Drosophila. J. Biol. Chem. 287 (2012), 21663–21672.
78. Stoll, H., Dengjel, J., Nerz, C., Gotz, F., Staphylococcus aureus deficient in lipidation of prelipoproteins is attenuated in growth and immune activation. Infect. Immun. 73 (2005), 2411–2423.
79. Sumiya, M., Super, M., Tabona, P., Levinsky, R.J., Arai, T., Turner, M.W., Summerfield, J.A., Molecular basis of opsonic defect in immunodeficient children. Lancet 337 (1991), 1569–1570.
80. Summerfield, J.A., Sumiya, M., Levin, M., Turner, M.W., Association of mutations in mannose binding protein gene with childhood infection in consecutive hospital series. BMJ 314 (1997), 1229–1232.
81. Super, M., Thiel, S., Lu, J., Levinsky, R.J., Turner, M.W., Association of low levels of mannan-binding protein with a common defect of opsonisation. Lancet 2 (1989), 1236–1239.
82. Takahashi, M., Ishida, Y., Iwaki, D., Kanno, K., Suzuki, T., Endo, Y., Homma, Y., Fujita, T., Essential role of mannose-binding lectin-associated serine protease-1 in activation of the complement factor D. J. Exp. Med. 207 (2010), 29–37.
83. Takahashi, K., Chang, W.C., Takahashi, M., Pavlov, V., Ishida, Y., La Bonte, L., Shi, L., Fujita, T., Stahl, G.L., Van Cott, E.M., Mannose-binding lectin and its associated proteases (MASPs) mediate coagulation and its deficiency is a risk factor in developing complications from infection, including disseminated intravascular coagulation. Immunobiology 216 (2011), 96–102.
84. Takahashi, K., Kurokawa, K., Moyo, P., Jung, D.J., An, J.H., Chigweshe, L., Paul, E., Lee, B.L., Intradermal immunization with wall teichoic acid (WTA) elicits and augments an anti-WTA IgG response that protects mice from methicillin-resistant Staphylococcus aureus infection independent of mannose-binding lectin status. PLoS One, 8, 2013, e69739.
85. Takeuchi, O., Akira, S., Pattern recognition receptors and inflammation. Cell 140 (2010), 805–820.
86. Takeuchi, O., Kaufmann, A., Grote, K., Kawai, T., Hoshino, K., Morr, M., Muhlradt, P.F., Akira, S., Cutting edge: preferentially the R-stereoisomer of the mycoplasmal lipopeptide macrophage-activating lipopeptide-2 activates immune cells through a toll-like receptor 2- and MyD88-dependent signaling pathway. J. Immunol. 164 (2000), 554–557.
87. Thomas, C.A., Li, Y., Kodama, T., Suzuki, H., Silverstein, S.C., El Khoury, J., Protection from lethal gram-positive infection by macrophage scavenger receptor-dependent phagocytosis. J. Exp. Med. 191 (2000), 147–156.
88. Torii, M., Kabat, E.A., Bezer, A.E., Separation of teichoic acid of staphylococcus aureus into two immunologically distinct specific polysaccharides with alpha- and beta-N-acetylglucosaminyl linkages respectively antigenicity of theichoic acids in man. J. Exp. Med. 120 (1964), 13–29.
89. Weidenmaier, C., Peschel, A., Teichoic acids and related cell-wall glycopolymers in Gram-positive physiology and host interactions. Nat. Rev. 6 (2008), 276–287.
90. Weidenmaier, C., Kokai-Kun, J.F., Kristian, S.A., Chanturiya, T., Kalbacher, H., Gross, M., Nicholson, G., Neumeister, B., Mond, J.J., Peschel, A., Role of teichoic acids in Staphylococcus aureus nasal colonization, a major risk factor in nosocomial infections. Nat. Med. 10 (2004), 243–245.
91. Weidenmaier, C., McLoughlin, R.M., Lee, J.C., The zwitterionic cell wall teichoic acid of Staphylococcus aureus provokes skin abscesses in mice by a novel CD4+ T-cell-dependent mechanism. PLoS One, 5, 2010, e13227.
92. Weis, W.I., Drickamer, K., Structural basis of lectin-carbohydrate recognition. Annu. Rev. Biochem. 65 (1996), 441–473.
93. Weis, W.I., Drickamer, K., Hendrickson, W.A., Structure of a C-type mannose-binding protein complexed with an oligosaccharide. Nature 360 (1992), 127–134.
94. Winstel, V., Liang, C., Sanchez-Carballo, P., Steglich, M., Munar, M., Broker, B.M., Penades, J.R., Nubel, U., Holst, O., Dandekar, T., Peschel, A., Xia, G., Wall teichoic acid structure governs horizontal gene transfer between major bacterial pathogens. Nat. Commun., 4, 2013, 2345.
95. Xia, Guoqing, Maier, Lisa, Sanchez-Carballo, Patricia, Li, Min, Otto, Michael, Holst, Otto, Peschel, Andreas, Glycosylation of wall teichoic acid in Staphylococcus aureus by TarM. J. Biol. Chem. 285 (2010), 13405–13415, 10.1074/jbc.M109.096172 originally published online February 25, 2010.